Skip to main content
SpringerLink
Log in

Chlorine dioxide gas mediated inactivation of the biofilm cells of

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

This study evaluated the chlorine dioxide (ClO2) gas mediated inactivation of the biofilm cells of foodborne pathogens on food contact surfaces. Biofilm cells of Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes were developed on stainless steel (SS) and high density polyethylene (HDPE) coupon surfaces, and 5-day-old biofilms were treated with ClO2 gas at 60 and 90% relative humidity (RH) for up to 20 min. With an increase in gas concentration and treatment time, significant differences (p < 0.05) were observed between reduction levels under different RH conditions. Treatment with 50 ppmv of ClO2 gas (60% RH) for 20 min resulted in log reductions from 2.08 to 4.62 and 2.08 to 4.41 of the biofilm cells of three pathogens on SS and HDPE surfaces, respectively. The levels of biofilm cells of E. coli O157:H7, S. Typhimurium, and L. monocytogenes on SS and HDPE surfaces were reduced to below the detection limit (0.48 log CFU/cm2) within 15, 20, and 20 min, respectively, when exposure to 50 ppmv of ClO2 gas at 90% RH.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data availability

The authors confirm that the data supporting the findings of this study are available within the article.

Abbreviations

SS:

Stainless steel

HDPE:

High density polyethylene

RH:

Relative humidity

EPS:

Extra polymeric substances

TSA:

Tryptic soy agar

TSB:

Tryptic soy broth

PBS:

Phosphate-buffered saline

PW:

Peptone water

SMAC:

Sorbitol MacConkey agar

XLD:

Xylose Lysine Desoxycholate agar

OAB:

Oxford agar base

References

  • Ban GH, Kang DH (2016) Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiol 55:47–54

    Article  CAS  Google Scholar 

  • Ban GH, Yoon H, Kang DH (2014) A comparison of saturated steam and superheated steam for inactivation of Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes biofilms on polyvinyl chloride and stainless steel. Food Control 40:344–350

    Article  CAS  Google Scholar 

  • Baumann AR, Martin SE, Feng H (2009) Removal of Listeria monocytogenes biofilms from stainless steel by use of ultrasound and ozone. J Food Prot 72:1306–1309

    Article  Google Scholar 

  • Bhagat A, Mahmoud BSM, Linton RH (2011) Effect of chlorine dioxide gas on Salmonella enterica inoculated on navel orange surfaces and its impact on the quality attributes of treated oranges. Foodborne Path Dis 8:77–85

    Article  CAS  Google Scholar 

  • Cappitelli F, Polo A, Villa F (2014) Biofilm formation in food processing environments is still poorly understood and controlled. Food Eng Rev 6:29–42

    Article  Google Scholar 

  • Chmielewski R, Frank J (2003) Biofilm formation and control in food processing facilities. Compr Rev Food Sci Food Saf 2:22–32

    Article  CAS  Google Scholar 

  • Cortés ME, Bonilla JC, Sinisterra RD (2011) Biofilm formation, control and novel strategies for eradication. Sci Against Microbial Pathog Commun Curr Res Technol Adv 2:896–905

    Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    Article  CAS  Google Scholar 

  • Gora SL, Rauch KD, Ontiveros CC, Stoddart AK, Gagnon GA (2019) Inactivation of biofilm-bound Pseudomonas aeruginosa bacteria using UVC light emitting diodes (UVC LEDs). Water Res 151:193–202

    Article  CAS  Google Scholar 

  • Govaert M, Smet C, Baka M, Janssens T, Van Impe J (2018) Influence of incubation conditions on the formation of model biofilms by Listeria monocytogenes and Salmonella Typhimurium on abiotic surfaces. J Appl Microbiol 125:1890–1990

    Article  CAS  Google Scholar 

  • Govaert M, Smet C, Walsh JL, Van Impe JFM (2019) Dual-species model biofilm consisting of Listeria monocytogenes and Salmonella Typhimurium: development and inactivation with cold atmospheric plasma (CAP). Front Microbiol 10:2524

    Article  Google Scholar 

  • Gupta P, Sarkar S, Das B, Bhattacharjee S, Tribedi P (2016) Biofilm, pathogenesis and prevention—a journey to break the wall: a review. Arch Microbiol 198:1–15

    Article  CAS  Google Scholar 

  • Han Y, Floros JD, Linton RH, Nielsen SS, Nelson PE (2001) Response surface modeling for the inactivation of Escherichia coli O157:H7 on green peppers (Capsicum annuum L.) by chlorine dioxide gas treatments. J Food Prot 64:1128–1133

    Article  CAS  Google Scholar 

  • Kim WJ, Kim SH, Kang DH (2020) Thermal and non-thermal treatment effects on Staphylococcus aureus biofilms formed at different temperatures and maturation periods. Food Res Int 137:109432

    Article  CAS  Google Scholar 

  • Korany AM, Hua Z, Green T, Hanrahan I, El-Shinawy SH, El-Kholy A et al (2018) Efficacy of ozonated water, chlorine, chlorine dioxide, quaternary ammonium compounds and peroxyacetic acid against Listeria monocytogenes biofilm on polystyrene surfaces. Front Microbiol 9:2296

    Article  Google Scholar 

  • Li X, Kim MJ, Bang WS, Yuk HG (2018) Anti-biofilm effect of 405-nm LEDs against Listeria monocytogenes in simulated ready-to-eat fresh salmon storage conditions. Food Control 84:513–521

    Article  CAS  Google Scholar 

  • Linton RH, Han Y, Selby TL, Nelson PE (2006) Gas-/vapor-phase sanitation (decontamination) treatments. In: Sapers GM, Gorny JR, Yousef AE (eds) Microbiology of fruits and vegetables. CRC Press Press, Boca Raton, FL

    Google Scholar 

  • Nam H, Seo HS, Bang J, Kim H, Beuchat LR, Ryu JH (2014) Efficacy of gaseous chlorine dioxide in inactivating Bacillus cereus spores attached to and in a biofilm on stainless steel. Int J Food Microbiol 188:122–127

    Article  CAS  Google Scholar 

  • Park SH, Kang DH (2015) Antimicrobial effect of chlorine dioxide gas against foodborne pathogens under differing conditions of relative humidity. LWT 60:186–191

    Article  CAS  Google Scholar 

  • Park SH, Kang DH (2017) Influence of surface properties of produce and food contact surfaces on the efficacy of chlorine dioxide gas for the inactivation of foodborne pathogens. Food Control 81:88–95

    Article  CAS  Google Scholar 

  • Park SH, Kim WJ, Kang DH (2018) Effect of relative humidity on inactivation of foodborne pathogens using chlorine dioxide gas and its residues on tomatoes. Lett Appl Microbiol 67:154–160

    Article  CAS  Google Scholar 

  • Srey S, Jahid IK, Ha SD (2013) Biofilm formation in food industries: a food safety concern. Food Control 31:572–585

    Article  Google Scholar 

  • Trinetta V, Linton RH, Morgan MT (2013) The application of high-concentration short-time chlorine dioxide treatment for selected specialty crops including Roma tomatoes (Lycopersicon esculentum), cantaloupes (Cucumis melo ssp. melo var. cantaloupensis) and strawberries (Fragaria × ananassa). Food Microbiol 34:296–302

    Article  CAS  Google Scholar 

  • U.S. Food and Drug Administration (FDA) Food Code (2017) Recommendations of the United States public health service and food and Drug administration. College Park, MD: U. S. Department of Health and Human Services. https://www.fda.gov/food/fda-food-code/food-code-2017. Accessed 27 June 2022

  • Vaid R, Linton RH, Morgan MT (2010) Comparison of inactivation of Listeria monocytogenes within a biofilm matrix using chlorine dioxide gas, aqueous chlorine dioxide and sodium hypochlorite treatments. Food Microbiol 27:979–984

    Article  CAS  Google Scholar 

  • Vandekinderen I, Devlieghere F, Van Camp J, Kerkaert B, Cucu T, Ragaert P et al (2009) Effects of food composition on the inactivation of foodborne microorganisms by chlorine dioxide. Int J Food Microbiol 131:138–144

    Article  CAS  Google Scholar 

  • Wang H, Cai L, Li Y, Xu X, Zhou G (2018) Biofilm formation by meat-borne Pseudomonas fluorescens on stainless steel and its resistance to disinfectants. Food Control 91:397–403

    Article  CAS  Google Scholar 

  • Wang R, Kalchayanand N, King DA, Luedtke BE, Bosilevac JM, Arthur TM (2014) Biofilm formation and sanitizer resistance of Escherichia coli O157:H7 strains isolated from “High Event Period” meat contamination. J Food Prot 77:1982–1987

    Article  Google Scholar 

  • Wei Q, Ma LZ (2013) Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int J Mol Sci 14:20983–21005

    Article  Google Scholar 

  • Xue Z, Sendamangalam VR, Gruden CL, Seo Y (2012) Multiple roles of extracellular polymeric substances on resistance of biofilm and detached clusters. Environ Sci Technol 46:13212–13219

    Article  CAS  Google Scholar 

Download references

Acknowledgements

All bacterial strains used in this study were kindly provided by Dong-Hyun Kang (Department of Food Science and Biotechnology at Seoul National University). This research was financed by the National Research Foundation of Korea (NRF) and Korea Forest Service.

Funding

This work was supported by the National Research Foundation of Korea (NRF) Grant funded by the Korea government(MSIT) (NRF-2020R1F1A1048617). This study was carried out with the support of 'R&D Program for Forest Science Technology (Project No. 2021332C10-2123A01)' provided by Korea Forest Service (Korea Forestry Promotion Institute).

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, Kongju National University, Yesan, Chungnam, 32439, Republic of Korea

    Seyeon Kim & Sanghyun Park

Authors
  1. Seyeon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanghyun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to this manuscript as; S-YK: Investigation, Writing—original draft. S-HP: Conceptualization, Writing—review & editing, Resources, Supervision, Funding acquisition.

Corresponding author

Correspondence to Sanghyun Park.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Consent for publication

We hereby provide consent for publishing the results presented in this manuscript.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, S., Park, S. Chlorine dioxide gas mediated inactivation of the biofilm cells of. J Food Sci Technol 59, 4863–4869 (2022). https://doi.org/10.1007/s13197-022-05574-2

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-022-05574-2

Keywords

Search

Navigation